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Phylogeography and Ecological Niche Modeling Unravel the Evolutionary

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Phylogeography and Ecological Niche Modeling Unravel the Evolutionary Phylogeography and ecological niche modeling unravel the evolutionary history of the African green toad, Bufotes boulengeri boulengeri (Amphibia: Bufonidae), through the Quaternary Violaine Nicolas, Abderrahmane Mataame, Pierre-André Crochet, Philippe Geniez, Soumia Fahd, Annemarie Ohler To cite this version: Violaine Nicolas, Abderrahmane Mataame, Pierre-André Crochet, Philippe Geniez, Soumia Fahd, et al.. Phylogeography and ecological niche modeling unravel the evolutionary history of the African green toad, Bufotes boulengeri boulengeri (Amphibia: Bufonidae), through the Quaternary. Journal of Zo- ological Systematics and Evolutionary Research, Wiley, 2018, 56 (1), pp.102-116. 10.1111/jzs.12185. hal-01724136 HAL Id: hal-01724136 https://hal.sorbonne-universite.fr/hal-01724136 Submitted on 6 Mar 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. 1 Phylogeography and ecological niche modelling unravel the evolutionary history of the 2 African green toad, Bufotes boulengeri boulengeri (Amphibia: Bufonidae), through the 3 Quaternary 4 5 Violaine NICOLAS1, Abderrahmane MATAAME2, Pierre-André CROCHET3, Philippe 6 GENIEZ4, Soumia FAHD5, Annemarie OHLER1 7 8 1 Institut de Systématique, Evolution, Biodiversité, ISYEB - UMR 7205 - CNRS, MNHN, 9 UPMC, EPHE, Muséum national d’Histoire naturelle, Sorbonne Universités, Paris, France. 10 [email protected], [email protected] 11 2 Institut Scientifique de Rabat, Rabat, Maroc. [email protected] 12 3 CEFE UMR 5175, CNRS, Université de Montpellier, Université Paul-Valéry Montpellier, 13 EPHE, Montpellier, France. [email protected] 14 4 PSL Research University, CEFE UMR 5175, CNRS, Université de Montpellier, Université 15 Paul-Valéry Montpellier, EPHE, Biogéographie et Ecologie des Vertébrés, Montpellier, 16 France. [email protected] 17 5 Laboratoire "Ecologie, Biodiversité et Environnement", Département de Biologie, Faculté 18 des Sciences de Tétouan, Université Abdelmalek Essaâdi, Tétouan, Maroc. 19 [email protected] 20 21 Corresponding author: Violaine NICOLAS 22 Tel: 00 33 1 40 79 48 52 23 [email protected] 24 25 Running title: Evolutionary history of the African green toad 26 27 Keywords 28 Amphibian - Ecological niche modelling - Genetic structure - Maghreb – Pleistocene 29 1 1 Abstract 2 Recent integration of ecological niche models in phylogeographic studies is improving our 3 understanding of the processes structuring genetic variation across landscapes. Previous 4 studies on the amphibian B. b. boulengeri uncovered a surprisingly weak intraspecific 5 differentiation across the Maghreb region. We widely sampled this species from Morocco to 6 Egypt, and sequenced one nuclear and three mitochondrial (mtDNA) genes to determine the 7 level of genetic variability across its geographic range. We evaluated these data with 8 ecological niche modelling to reveal its evolutionary history in response to climate change 9 during the Quaternary. Our results highlight some mtDNA phylogeographic structure within 10 this species, with one haplogroup endemic to coastal Morocco, and one haplogroup widely 11 distributed throughout North Africa. No or little genetic differentiation is observed between 12 isolated populations from the Hoggar Mountains, the Sabha district and the islands of 13 Kerkennah and Lampedusa, compared to others populations. This can be explained by the 14 expansion of the distribution range of B. b. boulengeri during glacial periods. This might have 15 facilitated the species’ dispersal and subsequent gene flow between most North African 16 localities. 17 18 Introduction 19 Green toads of the Bufotes viridis (Laurenti, 1768) species complex are widespread in the 20 Palearctic region where they have differentiated into several lineages (Batista et al. 2006; 21 Stöck et al. 2006; Stöck et al. 2008). Using two mitochondrial genes, Stöck et al. (2006) 22 suggested that at least five species can be recognised within this complex of species, but 23 evidence of reproductive isolation or even distinct nuclear gene pools is lacking for several of 24 these mitochondrial lineages. More detailed studies using mtDNA and two nuclear sequence 25 markers, sex-chromosomes, and additional morphological, phenological, and bioacoustic data 26 focused on the North African-Sicilian lineage (Stöck et al. 2008) demonstrated its 27 evolutionary distinctiveness and documented strong reproductive isolation from the Italian 28 mitochondrial lineage in Sicily. On the contrary, studies of contact zones between the younger 29 lineages viridis and balearicus (Boettger, 1880) revealed extensive introgression of nuclear 30 markers and lack of intrinsic reproductive isolation (Dufresnes et al. 2014). As a consequence 31 Speybroeck et al. (2016) recognised only the North African-Sicilian lineage as a valid species, 32 Bufotes boulengeri (Lataste, 1879), and proposed to postpone further species-level splits until 33 the situation in other contact zones is documented. According to these authors B. boulengeri 2 1 is subdivided in two subspecies: B. b. boulengeri and B. b. siculus (Stöck et al. 2008) 2 (availability of the nomen siculus is unclear, see Dubois et al. 2013; ICZN 2014). 3 The African green toad, Bufotes b. boulengeri, occurs as fragmented populations in North 4 Africa from the Moroccan Atlantic coast eastwards to the Nile valley in Egypt, including 5 several Mediterranean islands (Martínez-Solano et al. 2015). It is a characteristic inhabitant of 6 relatively arid, open landscapes (Beukema et al. 2013) but it can inhabit a wide range of 7 habitat: forested areas, scrubland, dry grassland, semi-deserts and deserts (Martínez-Solano et 8 al. 2015). Several highly isolated populations are known from Algeria (e.g. Hoggar 9 Mountains), Libya (Sabha district), as well as on the islands of Kerkennah and Lampedusa 10 (Figure 1). In Morocco it is most abundant on the Atlantic coast (as far south as Dakhla) and 11 in the High and Middle Atlas Mountains, with scattered populations in the north, north-east 12 and east of the country and in the northern Saharan margins (Beukema et al. 2013). The 13 species is mostly absent from the Rif Mountains, where it is limited to river corridors and is 14 absent from the mountain cores characterized by a more humid climate (Donaire et al. 2011). 15 While strong phylogeographic structure is commonly found in amphibian species across the 16 Maghreb region (Ben Hassine et al. 2016; Nicolas et al. 2015; Recuero et al. 2007; Vences et 17 al. 2014), previous studies on B. b. boulengeri uncovered a surprisingly weak intraspecific 18 differentiation over its geographic range (Batista et al. 2006; Stöck et al. 2006; Stöck et al. 19 2008). This is especially unexpected because fossil data indicates that the African green toad 20 has been present in North Africa since the beginning of the Pleistocene (2.5 Ma in Morocco, 21 (Bailon 2000). Climatic reconstructions and paleoenvironmental data show that North Africa 22 regularly shifted from wetter to drier climatic conditions throughout the Quaternary 23 (deMenocal 2004; Schuster et al. 2006; Tabel et al. 2016). This climatic instability led to 24 periodic modifications of habitats, such as contraction/ expansion of the Sahara desert, 25 emergence of more open habitats or deep modifications of hydrographic networks (Rognon 26 1989; Le Houérou 1997; Drake et al. 2011). Several geographical features, such as the Sahara 27 desert, the Atlas Mountains or the Moulouya River valley are known to have acted as barrier 28 to dispersal for many species and promoted diversification in several species or species 29 complexes ( Aulagnier and Thevenot 1986; Alvarez et al. 2000; Brown et al. 2002; Ben Faleh 30 et al. 2012; Douady et al. 2003; Escoriza et al. 2006; Fritz et al. 2006; Barata et al. 2008; 31 Nicolas et al. 2014). 32 In this study, we widely sampled African green toads from Morocco to Egypt (95 newly 33 collected individuals in Morocco, Algeria and Egypt, and 39 specimens from Algeria, Egypt, 34 Libya, Morocco, Tunisia and Lampedusa Island retrieved from GenBank) and sequenced 3 1 three mitochondrial (mtDNA) and one nuclear (nDNA) genes to determine the level of 2 genetic variability within B. b. boulengeri across its geographic range. We specifically tested 3 whether isolated populations from the Hoggar Mountains, the Sabha district and the islands of 4 Kerkennah and Lampedusa are genetically differentiated from others populations. Moreover, 5 we evaluated these genetic data with ecological niche modelling based on bioclimatic data to 6 reveal the evolutionary history of B. b. boulengeri in response to climate change during the 7 Quaternary. 8 9 Material and methods 10 DNA extraction, amplification and sequencing 11 Ninety-five newly collected individuals were included in this study (15 specimens from 12 Algeria, two from Egypt and 78 from Morocco; Supporting information Table S1). When 13 available, these specimens were deposited either at the Museum National d’Histoire Naturelle 14 (MNHN, Paris, France) or at the collection
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